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Research ArticleADULT BRAIN

Significance of Development and Reversion of Collaterals on MRI in Early Neurologic Improvement and Long-Term Functional Outcome after Intravenous Thrombolysis for Ischemic Stroke

M. Ichijo, E. Iwasawa, Y. Numasawa, K. Miki, S. Ishibashi, M. Tomita, H. Tomimitsu, T. Kamata, H. Fujigasaki, S. Shintani and H. Mizusawa
American Journal of Neuroradiology October 2015, 36 (10) 1839-1845; DOI: https://doi.org/10.3174/ajnr.A4384
M. Ichijo
aFrom the Department of Neurology and Neurological Science (M.I., E.I., Y.N., S.I., and H.M.)
eDepartment of Neurology, Musashino Red Cross Hospital (M.I., T.K.), Tokyo, Japan
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E. Iwasawa
aFrom the Department of Neurology and Neurological Science (M.I., E.I., Y.N., S.I., and H.M.)
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Y. Numasawa
aFrom the Department of Neurology and Neurological Science (M.I., E.I., Y.N., S.I., and H.M.)
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K. Miki
bDepartment of Endovascular Surgery (K.M.)
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S. Ishibashi
aFrom the Department of Neurology and Neurological Science (M.I., E.I., Y.N., S.I., and H.M.)
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M. Tomita
cClinical Research Center (M.T.), Tokyo Medical and Dental University, Tokyo, Japan
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H. Tomimitsu
dDepartment of Neurology, JA Toride Medical Center (H.T., S.S.), Ibaraki, Japan
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T. Kamata
eDepartment of Neurology, Musashino Red Cross Hospital (M.I., T.K.), Tokyo, Japan
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H. Fujigasaki
fDepartment of Internal Medicine (H.F.), Metropolitan Bokutoh Hospital, Tokyo, Japan.
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S. Shintani
dDepartment of Neurology, JA Toride Medical Center (H.T., S.S.), Ibaraki, Japan
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H. Mizusawa
aFrom the Department of Neurology and Neurological Science (M.I., E.I., Y.N., S.I., and H.M.)
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  • Fig 1.
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    Fig 1.

    PCA laterality sign and hyperintense vessels on MR images. A, MRA shows an occlusion of the M1 portion of the left MCA and signal extent of the ipsilateral PCA (arrowhead). B, FLAIR MR imaging shows hyperintense vessels (arrows) in 8 of 10 axial sections.

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    Fig 2.

    Reversion of collateral signs on MR images. MRA (A and C) and FLAIR MR imaging (B and D) of a representative patient who experienced early neurologic improvement after IV rtPA. PCA laterality (arrowheads) and hyperintense vessels (dotted circles) were observed before treatment (A and B) but disappeared after thrombolysis (C and D), indicating the reversion of collaterals.

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    Fig 3.

    Distribution of the hyperintense vessel (HV) score before and after rtPA treatment. Most patients (39 of 48, 81%) were initially classified in the middle and high HV score group before treatment (A); however, the number of patients with a middle or high HV score dramatically decreased after thrombolysis (B).

Tables

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    Table 1:

    Characteristics of patients with and without reversion of collateralsa

    Reversion of CollateralsP Value
    Yes (n = 25)No (n = 23)
    Age (median) (IQR)78 (71–81)79 (68–86).52
    Male sex (No.) (%)13 (52)13 (57).78
    mRS 0–1 before stroke (No.) (%)25 (100)22 (96).48
    Cardiovascular risk factors (No.) (%)
        Hypertension15 (60)13 (57)1
        Diabetes mellitus7 (28)3 (13).29
        Hyperlipidemia4 (16)7 (30).31
        Atrial fibrillation21 (84)13 (57).057
        Congestive heart failure5 (20)4 (17)1
        Previous stroke6 (24)6 (26)1
        Smoking9 (36)9 (41).77
    Past medication at stroke onset (No.) (%)
        Antiplatelet therapy7 (28)8 (35).76
        Anticoagulant therapy5 (20)4 (17)1
        Antihypertensive therapy13 (52)10 (44).58
        Statin therapy2 (8)4 (17).41
    Stroke etiology (No.) (%)
        Cardioembolism19 (76)11 (48).07
        Atherosclerosis4 (16)8 (35).19
        Other or undetermined2 (8)4 (17).41
    Severity of stroke at arrival (median) (IQR)
        Initial GCS13 (11–14)12 (10–14).62
        Initial DWI volume (mL)21.6 (13.8–42.5)22.9 (10.6–41.1).63
        DWI ASPECTS at arrival8 (7–9)8 (6–8).72
        Initial NIHSS score17 (14–24)16 (11–21).35
    Duration between 2 MRI scans (days)7 (5–9)6 (3–8).2
    Neurologic and radiologic outcome after rtPA (median) (IQR)
        24-hr NIHSS7 (2–12)11 (6–17).022b
        7-day NIHSS4 (1–8)8 (3–14).008c
        Hemorrhagic transformation6 (24)10 (43).22
        Successful recanalization23 (92)8 (35)<.001d
        Follow-up CT ASPECTS8 (6.5–9)6 (4–8).017b
            M1 to M6 area in ASPECTS5 (4–6)3 (2–6).021b
            C, I, L, IC area in ASPECTS3 (2.5–4)3 (2–3).12
        mRS 0–1 at 3 mo (No.) (%)16 (64)8 (35).043b
    • Note:—GCS indicates Glasgow Coma Scale; C, caudate nucleus; I, insular cortex; L, lenticular nucleus; IL, internal capsule.

    • ↵a For continuous variables, the median and P values (Mann-Whitney U test) are shown. The resulting proportions and the P values (Fisher exact test with Yates correction, when appropriate) are shown.

    • ↵b P < .05.

    • ↵c P < .01.

    • ↵d P < .001 was considered significant.

    • View popup
    Table 2:

    Comparison of the presence and absence of early neurologic improvement after IV rtPA in patients with proximal middle cerebral artery occlusiona

    Early Neurologic ImprovementP Value
    Yes (n = 22)No (n = 26)
    Age (yr) ( median) (IQR)78.5 (74–81)78.5 (68–84).92
    Male sex (No.) (%)10 (45)16 (62).38
    mRS 0–1 before stroke (No.) (%)22 (100)25 (96)1
    NIHSS score at arrival (median) (mean)17.9 ± 8.116.0 ± 5.7.29
    Systolic blood pressure (mean)161.3 ± 29.6155.0 ± 30.8.91
    Diastolic blood pressure (mean)88.5 ± 26.178.3 ± 21.9.19
    Temperature (°C) (mean)36.3 ± 0.436.2 ± 0.7.75
    Cardiovascular risk factors (No.) (%)
        Hypertension14 (64)14 (54).57
        Diabetes mellitus7 (27)4 (15).48
        Hyperlipidemia5 (23)6 (23)1
        Atrial fibrillation19 (86)15 (58).054
        Congestive heart failure4 (18)5 (19)1
        Previous stroke5 (23)7 (27)1
        Smoking6 (27)12 (48).23
    Past medication at stroke onset (No.) (%)
        Antiplatelet therapy8 (36)7 (27).54
        Anticoagulant therapy4 (18)5 (19)1
        Antihypertensive therapy14 (64)9 (35).08
        Statin therapy2 (9)4 (15).67
    Stroke etiology (No.) (%)
        Cardioembolism17 (77)13 (50).074
        Atherosclerosis4 (18)8 (31).5
        Other or undetermined1 (5)5 (19).2
    Imaging analysis
        Initial DWI volume (mL) (median) (IQR)19.8 (11.5–42.3)22.7(13.9–41.2).26
        DWI ASPECTS at arrival (median) (IQR)8 (6.75–9)8 (6.75–8).33
        MCA M1 occlusion (No.) (%)18 (82)17 (65).33
        Development of collaterals at arrival (No.) (%)c15 (68)9 (35).042b
    Stroke outcome
        Follow-up CT ASPECTS (median) (IQR)8 (6–9.25)6 (4.75–8).004d
        mRS 0–1 at 3 mo (No.) (%)16 (73)8 (31).008d
    • ↵a For continuous variables, the median and P values (Mann-Whitney U test) are shown. The resulting proportions and the P values (Fisher exact test with Yates correction, when appropriate) are shown.

    • ↵b P < .05.

    • ↵c The development of collaterals was defined as positive in the presence of PCA laterality and an HV score of ≥5 on initial MRI.

    • ↵d P <.01 was considered significant.

    • View popup
    Table 3:

    Univariate analyses and multivariate logistic regression analysis for the association of early neurologic improvement after IV rtPA in patients with proximal middle cerebral artery occlusion

    Crude ORP ValueAdjusted ORP Value
    (95% CI)(95% CI)
    Age (yr)0.99 (0.95–1.06).911.00 (0.94–1.06).95
    Male sex0.52 (0.16–1.63).26
    History of atrial fibrillation4.64 (1.20–23.36).025a5.32 (1.16–32.1).031a
    NIHSS score at arrival1.04 (0.88–1.04).341.02 (0.89–1.09).72
    DWI ASPECTS at arrival1.16 (0.80–1.73).44
    Time to rtPA administration0.99 (0.97–1.02).491.00 (0.97–1.03).84
    Development of collaterals at arrivalb4.0 (1.25–14.27).019a4.82 (1.34–19.98).015a
    • ↵a P < .05 was considered significant.

    • ↵b The development of collaterals was defined as positive in the presence of PCA laterality positivity and an HV score of ≥5 on initial MRI.

    • c Adjusted for age, history of atrial fibrillation, NIHSS score at arrival, and time to rtPA administration.

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American Journal of Neuroradiology: 36 (10)
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M. Ichijo, E. Iwasawa, Y. Numasawa, K. Miki, S. Ishibashi, M. Tomita, H. Tomimitsu, T. Kamata, H. Fujigasaki, S. Shintani, H. Mizusawa
Significance of Development and Reversion of Collaterals on MRI in Early Neurologic Improvement and Long-Term Functional Outcome after Intravenous Thrombolysis for Ischemic Stroke
American Journal of Neuroradiology Oct 2015, 36 (10) 1839-1845; DOI: 10.3174/ajnr.A4384

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Significance of Development and Reversion of Collaterals on MRI in Early Neurologic Improvement and Long-Term Functional Outcome after Intravenous Thrombolysis for Ischemic Stroke
M. Ichijo, E. Iwasawa, Y. Numasawa, K. Miki, S. Ishibashi, M. Tomita, H. Tomimitsu, T. Kamata, H. Fujigasaki, S. Shintani, H. Mizusawa
American Journal of Neuroradiology Oct 2015, 36 (10) 1839-1845; DOI: 10.3174/ajnr.A4384
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